Premotor cortex and the conditions for movement in monkeys (Macaca fascicularis)

doi:10.1016/0166-4328(85)90035-X

Behavioural Brain Research

Volume 18, Issue 3, December 1985, Pages 269-277

https://doi.org/10.1016/0166-4328(85)90035-X Get rights and content

Abstract

Cortical association areas direct their influence on motor cortex via premotor and supplementary motor cortex. In the present experiment premotor cortex was removed bilaterally in monkeys. The monkeys were unable to relearn a visual conditional motor task on which the correct action is specified by visual cues. It was shown that the same monkeys were able to learn a non-motor visual conditional task on which the visual cues specified which object should be chosen. It is concluded that the monkeys are only impaired when they must recall a movement from memory on the basis of a visual cue.

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Cited by (182)

The dorsal premotor cortex encodes the step-by-step planning processes for goal-directed motor behavior in humans
2022, NeuroImage
Citation Excerpt :
From this perspective, the premotor and parietal cortices are candidate neural substrates for visuo-goal behavior. Previous studies have revealed that the dorsal premotor cortex (PMd) plays a central role in conditional visuomotor behavior, in which a visual signal is arbitrarily linked with physical parameters (Amiez et al., 2006; Boussaoud, 2001; Boussaoud et al., 1993; Boussaoud and Wise, 1993; Cisek and Kalaska, 2005; Grafton et al., 1998; Halsband and Passingham, 1985; Kurata and Hoffman, 1994; Passingham, 1993; Petrides, 1986; Simon et al., 2002; Toni et al., 2002, 2001, 1999). However, the conventional conditional visuomotor paradigm does not examine the process of generating a behavioral goal because the physical parameters of an action are uniquely specified immediately after the visual stimulus is presented.
The dorsal premotor cortex (PMd) plays an essential role in visually guided goal-directed motor behavior. Although there are several planning processes for achieving goal-directed behavior, the separate neural processes are largely unknown. Here, we created a new visuo-goal task to investigate the step-by-step planning processes for visuomotor and visuo-goal behavior in humans. Using functional magnetic resonance imaging, we found activation in different portions of the bilateral PMd during each processing step. In particular, the activated area for rule-based visuomotor and visuo-goal mapping was located at the ventrorostral portion of the bilateral PMd, that for action plan specification was at the dorsocaudal portion of the left PMd, that for transformation was at the rostral portion of the left PMd, and that for action preparation was at the caudal portion of the bilateral PMd. Thus, the left PMd was involved throughout all of the processes, but the right PMd was involved only in rule-based visuomotor and visuo-goal mapping and action preparation. The locations related to each process were generally spatially separated from each other, but they overlapped partially. These findings revealed that there are functional subregions in the bilateral PMd in humans and these subregions form a functional gradient to achieve goal-directed behavior.
The motor engram as a dynamic change of the cortical network during early sequence learning: An fMRI study
2020, Neuroscience Research
Citation Excerpt :
A previous non-human primate study (Hoshi and Tanji, 2006) showed that PMd neurons could retain and combine information about a spatial target and effector to generate the information that specifies a forthcoming action. Clinical lesions of the PMd in humans disrupted the ability to use arbitrary cues to withhold or perform a particular movement (Petrides, 1982,1985; Halsband and Passingham, 1982,1985). A meta-analysis of human functional neuroimaging studies by Witt et al. (2008) showed that the visually paced finger-tapping tasks activated bilateral PMd, whereas self-paced tasks activated the left PMd and auditory-paced tasks the right.
Neural substrates of motor engrams in the human brain are hard to identify because their dormant states are difficult to discriminate. We utilized eigenvector centrality (EC) to measure the network information that accumulates as an engram during learning. To discriminate engrams formed by emphasis on speed or accuracy, we conducted functional MRI on 58 normal volunteers as they performed a sequential finger-tapping task with the non-dominant left hand. Participants alternated between performing a tapping sequence as quickly as possible (maximum mode) or at a constant speed of 2 Hz, paced by a sequence-specifying visual cue (constant mode). We depicted the formation of the motor engram by characterizing the dormant state as the increase in EC of the resting epoch throughout the training course, and the ecphory, or activated state, as the increment in EC during the task epoch relative to the alternated resting epoch. We found that a network covering the left anterior intraparietal sulcus and inferior parietal lobule represented the engram for the speed of execution, whereas bilateral premotor cortex and right primary motor cortex represented the sequential order of movements. This constitutes the first demonstration of learning-mode specific motor engrams formed by only 30 min of training.
Brain activation profiles during kinesthetic and visual imagery: An fMRI study
2016, Brain Research
The aim of this study was to identify brain regions involved in motor imagery and differentiate two alternative strategies in its implementation: imagining a motor act using kinesthetic or visual imagery. Fourteen adults were precisely instructed and trained on how to imagine themselves or others perform a movement sequence, with the aim of promoting kinesthetic and visual imagery, respectively, in the context of an fMRI experiment using block design. We found that neither modality of motor imagery elicits activation of the primary motor cortex and that each of the two modalities involves activation of the premotor area which is also activated during action execution and action observation conditions, as well as of the supplementary motor area. Interestingly, the visual and the posterior cingulate cortices show reduced BOLD signal during both imagery conditions. Our results indicate that the networks of regions activated in kinesthetic and visual imagery of motor sequences show a substantial, while not complete overlap, and that the two forms of motor imagery lead to a differential suppression of visual areas.
The effect of speech distortion on the excitability of articulatory motor cortex
2016, NeuroImage
It has become increasingly evident that human motor circuits are active during speech perception. However, the conditions under which the motor system modulates speech perception are not clear. Two prominent accounts make distinct predictions for how listening to speech engages speech motor representations. The first account suggests that the motor system is most strongly activated when observing familiar actions (Pickering and Garrod, 2013). Conversely, Wilson and Knoblich's account asserts that motor excitability is greatest when observing less familiar, ambiguous actions (Wilson and Knoblich, 2005). We investigated these predictions using transcranial magnetic stimulation (TMS). Stimulation of the lip and hand representations in the left primary motor cortex elicited motor evoked potentials (MEPs) indexing the excitability of the underlying motor representation. MEPs for lip, but not for hand, were larger during perception of distorted speech produced using a tongue depressor, relative to naturally produced speech. Additional somatotopic facilitation yielded significantly larger MEPs during perception of lip-articulated distorted speech sounds relative to distorted tongue-articulated sounds. Critically, there was a positive correlation between MEP size and the perception of distorted speech sounds. These findings were consistent with predictions made by Wilson & Knoblich (Wilson and Knoblich, 2005), and provide direct evidence of increased motor excitability when speech perception is difficult.
Understanding bimanual coordination across small time scales from an electrophysiological perspective
2014, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
Invasive recordings showed that the prefrontal cortex and the pre-motor dorsal (PMd) area generate CNV (Hamano et al., 1997; Ikeda et al., 1999). In particular, PMd is linked to action selection during motor preparation, as shown in studies on monkeys (Halsband and Passingham, 1985) and humans (Grafton et al., 1998). Furthermore, in a repetitive transcranial magnetic stimulation (rTMS) study, perturbation to PMd induced changes in CNV, confirming its link to motor preparation (Lu et al., 2012).
Bimanual movement involves a variety of coordinated functions, ranging from elementary patterns that are performed automatically to complex patterns that require practice to be performed skillfully. The neural dynamics accompanying these coordination patterns are complex and rapid. By means of electro- and magneto-encephalographic approaches, it has been possible to examine these dynamics during bimanual coordination with excellent temporal resolution, which complements other neuroimaging modalities with superb spatial resolution. This review focuses on EEG/MEG studies that unravel the processes involved in movement planning and execution, motor learning, and executive functions involved in task switching and dual tasking. Evidence is presented for a spatio-temporal reorganization of the neural networks within and between hemispheres to meet increased task difficulty demands, induced or spontaneous switches in coordination mode, or training-induced neuroplastic modulation in coordination dynamics. Future theoretical developments will benefit from the integration of research techniques unraveling neural activity at different time scales. Ultimately this work will contribute to a better understanding of how the human brain orchestrates complex behavior via the implementation of inter- and intra-hemispheric coordination networks.
Testing the model of caudo-rostral organization of cognitive control in the human with frontal lesions
2014, NeuroImage
Citation Excerpt :
Damage to the lateral and dorsal premotor region significantly contributed to impairments in sensory control. Consistent with the present results, previous studies in human and non-human primates using conditional associative tasks have demonstrated that the lateral premotor cortex is crucial for sensorimotor associative learning but not for motor execution per se (Halsband and Freund, 1990; Halsband and Passingham, 1982, 1985; Passingham, 1985; Petrides, 1982; Wise et al., 1983). Further studies have also shown that sensorimotor associative learning involves the dorsal rather than the ventral portion of the lateral premotor cortex (Boussaoud and Wise, 1993; Kurata, 1994; Kurata and Hoffman, 1994).
The cascade model of cognitive control, mostly relying on functional neuroimaging studies, stipulates that the lateral frontal cortex (LFC) is organized as a cascade of executive processes involving three levels of cognitive control, implemented in distinct LFC areas from the premotor to the anterior prefrontal regions. The present experiment tested this model in patients with LFC lesions and studied the hierarchy of executive functions along the caudo-rostral axis, i.e. the respective roles of the different LFC areas in the control of behavior. Voxel-based lesion-symptom mapping and region of interest group analyses were conducted in 32 patients with focal LFC lesions who performed cognitive tasks assessing the cascade model. We first showed that three different LFC areas along the caudo-rostral axis subserved three distinct control levels, whose integrity is necessary for adaptive behavior. Second, we found that prefrontal cognitive control has an asymmetric organization: higher control processes involving more anterior prefrontal regions rely on the integrity of lower control processes in more posterior regions, while lower control processes can operate irrespective of the integrity of higher control processes. Altogether, these findings support a caudo-rostral cascade of executive processes from premotor to anterior prefrontal regions.

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Behavioural Brain Research

Abstract

References (30)

Topographic projections from the prefrontal cortex to the postarcuate area in the rhesus monkey, studied by retrograde axonal transport of horseradish peroxidase

Neurosci. Lett.

Further observations on corticofrontal connections in the rhesus monkey

Brain Res.

Premotor cortex and instrumental behaviour in monkeys

Physiol. Behav.

The role of premotor and parietal cortex in the direction of action

Brain Res.

Cortical motor representation of the laryngeal muscles in Macaca mulatta

Brain Res.

Regional distribution of functions in parietal association area 7 of the monkey

Brain Res.

A comment on the center for vertical eye movements in the medial prerubral subthalamic region of the monkey considering some of its frontal cortical afferents

Neurosci. Lett.

Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized ‘premotor areas’

Brain Res.

Association areas of the cerebral cortex

Trends Neurosci.

Motor conditional associative-learning after selective prefrontal lesions in the monkey

Behav. Brain Res.

Deficits in non-spatial conditional associative learning after periarcuate lesions in the monkey

Behav. Brain Res.

Organization of afferent input to subdivisions of area 8 in the rhesus monkey

J. Comp. Neurol.

Intracortical connectivities of somatic sensory and motor areas: multiple cortical pathways in monkeys

Primate frontal eye fields: single neurons discharging before saccades

J. Neurophysiol.

Motor functions of the basal ganglia

Cited by (182)

The dorsal premotor cortex encodes the step-by-step planning processes for goal-directed motor behavior in humans

The motor engram as a dynamic change of the cortical network during early sequence learning: An fMRI study

Brain activation profiles during kinesthetic and visual imagery: An fMRI study

The effect of speech distortion on the excitability of articulatory motor cortex

Understanding bimanual coordination across small time scales from an electrophysiological perspective

Testing the model of caudo-rostral organization of cognitive control in the human with frontal lesions

Research paperPremotor cortex and the conditions for movement in monkeys (Macaca fascicularis)

Abstract

Neurosci. Lett.

Brain Res.

Physiol. Behav.

Brain Res.

Brain Res.

Brain Res.

Neurosci. Lett.

Brain Res.

Trends Neurosci.

Behav. Brain Res.

Behav. Brain Res.

Organization of afferent input to subdivisions of area 8 in the rhesus monkey

J. Comp. Neurol.

Intracortical connectivities of somatic sensory and motor areas: multiple cortical pathways in monkeys

Primate frontal eye fields: single neurons discharging before saccades

J. Neurophysiol.

Motor functions of the basal ganglia

Research paper
Premotor cortex and the conditions for movement in monkeys (Macaca fascicularis)